EmrE, the smallest ion-coupled transporter, provides a unique paradigm for structure-function studies

Journal of Experimental Biology

Volumn 200, Issue 2, 1997, Pages 335-341

  Schuldiner, Shimon ^a   Lebendiker, Mario ^a   Yerushalmi, Hagit ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

cysteine; drug resistance; energy coupling; Escherichia coli; H+ transport; methyl viologen; MiniTexans; multidrug transporters; structure

Indexed keywords

EID: 0030939276     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (36)

1. AHMED, M., BORSCH, C. M., TAYLOR, S. S., VAZQUEZLASLOP, N. AND NEYFAKH, A. A. (1994). A protein that activates expression of a multidrug efflux transporter upon binding the transporter substrates. J. biol. Chem. 269, 28506-28513.
2. AKABAS. M., KAUFMANN, C., ARCHDEACON, P. AND KARLIN, A. (1994a). Identification of acetylcholine receptor channel-lining residues in the entire M2 segment of the a-subunit: implications for the secondary structure and for the locations of the gate and a selectivity filter. Neuron 13, 919-927.
3. AKABAS, M., KAUFMANN, C., COOK, T. AND ARCHDEACON, P. (1994b). Amino acid residues lining the chloride channel of the cystic fibrosis transmembrane conductance regulator. J. biol. Chem. 269, 14865-14868.
4. ARKIN. I., RUSS, W., LEBENDIKER, M. AND SCHULDINER, S. (1996). Determining the secondary structure and orientation of EmrE, a multi-drug transporter, indicates a transmembrane four helix bundle. Biochemistry, N.Y. 35, 7233-7238.
5. BANNER, D. W., CESARENI, G. AND TSERNOGLOU, D. J. (1987). Structure of the ColE1 rop protein at 1.7 Å resolution. Molec. Biol. 196, 657-675.
6. DOIGE, C. A. AND AMES, G. F. L. (1993). ATP-dependent transport systems in bacteria and humans - relevance to cystic fibrosis and multidrug resistance. A. Rev. Microbiol. 47, 291-319.
7. ENGELMAN, D., STEITS, T. AND GOLDMAN, A. (1986). Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. A. Rev. biophys. Chem. 15, 321-353.
8. FINZEL, B. C., WEBER, P. C., HARDMAN, K. D. AND SALEMME, F. R. (1985). Structure of ferricytochrome c′ from Rhosospirillum molischianum at 167 Å resolution. J. molec. Biol. 186, 627-643.
9. FOX, C. AND KENNEDY. E. (1965). Specific labeling and partial purification of the M protein, a component of the β-galactoside transport system of Escherichia coli. Proc. natn. Acad. Sci. U.S.A. 54, 891-899.
10. 0 ATP synthase. Biochemistry, N.Y. 32, 12167-12177.
11. 0 ATP synthase. Biochemistry, N.Y. 34, 1635-1645.
12. GRINIUS, L., DREGUNIENE, G., GOLDBERG, E. B., LIAO, C. H. AND PROJAN, S. J. (1992). A staphylococcal multidrug resistance gene product is a member of a new protein family. Plasmid 27, 119-129.
13. GRINIUS, L. AND GOLDBERG, E. (1994). Bacterial multidrug resistance is due to a single membrane protein which functions as a drug pump. J. biol. Chem. 269, 29998-30004.
14. GRUNDEMANN, D., GORBOULEV, V., GAMBARYAN, S., VEYHL, M. AND KOEPSELL, H. (1994). Drug excretion mediated by a new prototype of polyspecific transporter. Nature 372, 549-552.
15. IWATA, S., OSTERMEIER, C., LUDWIG, B. AND MICHEL, H. (1995). Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660-669.
16. LANYI, J. K. (1995). Bacteriorhodopsin as a model for proton pumps. Nature 375, 461-463.
17. LEBENDIKER, M. AND SCHULDINER, S. (1996). Identification of residues in the translocation pathway of EmrE, a multidrug antiporter from Escherichia coli. J. biol. Chem. 271, 21193-21199.
18. LEDERER, F., GLATIGNY, A., BETHGE, P. H., BELLAMY, H. D. AND MATHEWS, F. S. (1981). Improvement of the 2.5 Å resolution model of cytochrome b562 by redetermining the primary structure and using molecular graphics. J. molec. Biol. 148, 427-448.
19. LOMOVSKAYA, O., LEWIS, K. AND MATIN, A. (1995). EmrR is a negative regulator of the Escherichia coli multidrug resistance pump EmrAB. J. Bacteriol. 177, 2328-2334.
20. MIDGLEY, M. (1987). An efflux system for cationic dyes and related compounds in Escherichia coli. Microbiol. Sci. 4, 125-127.
21. MORIMYO, M., HONGO, E., HAMA-INABA, H. AND MACHIDA, I. (1992). Cloning and characterization of the mvrC gene of Escherichia coli K12 which confers resistance against methyl viologen toxicity. Nucleic Acids Res. 20, 3159-3165.
22. OKAMURA, M. AND FEHER, G. (1992). Proton transfer in reaction centers from photosynthetic bacteria. A. Rev. Biochem. 61, 861-896.
23. 15N NMR spectroscopy. Eur. J. Biochem. 219, 887-896.
24. PAULSEN, I., BROWN, M., DUNSTAN, S. AND SKURRAY, R. (1995). Molecular characterization of the staphylococcal multidrug resistance export protein QacC. J. Bacteriol. 177, 2827-2833.
25. PAULSEN, I., SKURRAY, R., TAM, R., SAIER, M., TURNER, R., WEINER, J., GOLDBERG, E. AND GRINIUS, L. (1996). The SMR family: a novel family of multidrug efflux proteins involved with the efflux of lipophilic drugs. Molec. Microbiol. 19, 1167-1175.
26. PUREWAL, A. S. (1991). Nucleotide sequence of the ethidium efflux gene from Escherichia coli. FEMS Microbiol. Lett. 82, 229-232.
27. RUETZ, S. AND GROS, P. (1995). Phosphatidylcholine translocase: a physiological role for the mdr2 gene. Cell 77, 1071-1081.
28. SCHINKEL, A. H., SMIT, J. J. M., VAN TELLINGEN, O., BEIJNEN, J. H., WAGENAAR, E., VAN DEEMTER, L., MOL. C., VAN DEN VALK, M., ROBANUS-MAANDAG, E., RIELE, H., BERNS, A. AND BORST, P. (1995). Disruption of the mouse mdr1a p-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77, 491-502.
29. SCHULDINER, S., SHIRVAN, A. AND LINIAL, M. (1995). Vesicular neurotransmitter transporters: from bacteria to human. Physiol. Rev. 75, 369-392.
30. SHERIFF, S., HENDRICKSON, W. A. AND SMITH, J. L. (1987). Structure of myohemerythin in the azidomet state at 1.7/1.3 Å resolution. J. molec. Biol. 197, 273-296.
31. WU, J. AND KABACK, H. (1994). Cysteine 148 in the lactose permease of E. coli is a component of the substrate binding site. II. Site directed fluorescence studies. Biochemistry N.Y. 33, 12166-12171.
32. XU, M. AND AKABAS, M. (1993). Amino acids lining the channel of the γ-aminobutyric acid type a receptor identified by cysteine substitution. J. biol. Chem. 268, 21505-21508.
33. YAN, R. T. AND MALONEY, P. C. (1993). Identification of a residue in the translocation pathway of a membrane carrier. Cell 75, 37-44.
34. YAN, R. T. AND MALONEY, P. C. (1995). Residues in the pathway through a membrane transporter. Proc. natn. Acad. Sci. U.S.A. 92, 5973-5976.
35. + and is soluble in organic solvents. J. biol. Chem. 270, 6856-6863.
36. YERUSHALMI, H., LEBENDIKER, M. AND SCHULDINER, S. (1996). Negative dominance studies demonstrate the oligomeric structure of EmrE, a multidrug antiporter from Escherichia coli. J. biol. Chem. (in press).